Trees - Structure and Function

Source-driven remobilizations of nutrients within stem wood in Eucalyptus grandis plantations

--Manuscript Draft-Manuscript Number: Full Title: Article Type: Keywords: Corresponding Author: Source-driven remobilizations of nutrients within stem wood in Eucalyptus grandis plantations Original Paper Resorption; trunk; potassium; sodium; eucalypt; retranslocation. Jean-Paul Laclau CIRAD Montpellier, FRANCE

Corresponding Author Secondary Information: Corresponding Author's Institution: Corresponding Author's Secondary Institution: First Author: First Author Secondary Information: Order of Authors: Carlos Roberto Sette Jr, Dr. Jean-Paul Laclau Mario Tomazello Filho, Pr. Rildo Moreira Moreira Jean-Pierre Bouillet, Dr. Julio Cesar Raposo de Almeida, Dr. Order of Authors Secondary Information: Abstract: Nutrient remobilizations in tree ligneous components have been little studied in tropical forests. A complete randomized block design was installed in Brazilian eucalypt plantations to quantify the remobilizations of phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg) and sodium (Na) within stem wood. Three treatments were studied: Control with neither K nor Na addition (C), 3 kmol ha-1 K applied (+K), and 3 kmol ha-1 Na applied (+Na). Biomass and nutrient contents were measured in the stem wood of 8 trees destructively sampled at 1, 2, 3 and 4 years after planting in each treatment and annual rings were localized on disks of wood sampled every 3 meters in half of the trees. Chemical analyses and wood density measurements were performed individually for each ring per level and per tree sampled. Nutrient remobilizations in annual rings were calculated through mass balance between two successive ages. Our results show that nutrient remobilizations within stem wood were mainly source-driven. Potassium and Na additions largely increased their concentration in the outer rings as well as the amounts remobilized in the first 2 years after the wood formation. The amount of Na remobilized in annual rings was 15% higher in +Na than in +K the 4th year after planting despite a 34% higher production of stem wood in +K leading to a much higher nutrient sink. A partial substitution of K by Na in the remobilizations within stem wood might contribute to enhancing Eucalyptus grandis growth in K-depleted soils. E.K.S. Nambiar, Dr. CSIRO Sadu.Nambiar@csiro.au P. Meerts pmeerts@ulb.ac.be
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Source-driven remobilizations of nutrients within stem wood in Eucalyptus grandis plantations Carlos Roberto Sette Jr1,2, Jean-Paul Laclau3,4,*, Mario Tomazello Filho2, Rildo Moreira e Moreira2, Jean-Pierre Bouillet3,2, Julio Cesar Raposo de Almeida5

UFG. Federal University of Gois. Forest Engineer Department. CEP 74690-900

Goinia. GO. Brazil

2

USP. University of So Paulo. ESALQ. Forest Science Department. Piracicaba. SP.

CEP 13418-900. Brazil

3

CIRAD. UMR 111. Ecologie Fonctionnelle & Biogochimie des Sols & Agro-

cosystmes. F-34060 Montpellier. France.

4

UNESP. Universidade Estadual Paulista. Cincia Florestal. Botucatu SP. CEP 18610-

307. Brazil.
5

University of Taubat, Taubat, Brazil.

Corresponding author (laclau@cirad.fr)

2 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 Key words: Resorption; trunk; potassium; sodium; eucalypt; retranslocation. Abstract: Nutrient remobilizations in tree ligneous components have been little studied in tropical forests. A complete randomized block design was installed in Brazilian eucalypt plantations to quantify the remobilizations of phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg) and sodium (Na) within stem wood. Three treatments were studied: Control with neither K nor Na addition (C), 3 kmol ha-1 K applied (+K), and 3 kmol ha-1 Na applied (+Na). Biomass and nutrient contents were measured in the stem wood of 8 trees destructively sampled at 1, 2, 3 and 4 years after planting in each treatment and annual rings were localized on disks of wood sampled every 3 meters in half of the trees. Chemical analyses and wood density measurements were performed individually for each ring per level and per tree sampled. Nutrient remobilizations in annual rings were calculated through mass balance between two successive ages. Our results show that nutrient remobilizations within stem wood were mainly source-driven. Potassium and Na additions largely increased their concentration in the outer rings as well as the amounts remobilized in the first 2 years after the wood formation. The amount of Na remobilized in annual rings was 15% higher in +Na than in +K the 4th year after planting despite a 34% higher production of stem wood in +K leading to a much higher nutrient sink. A partial substitution of K by Na in the remobilizations within stem wood might contribute to enhancing Eucalyptus grandis growth in Kdepleted soils.

3 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 INTRODUCTION Reviewing the ecophysiological relevance of nitrogen (N) remobilizations within trees, Millard and Grelet (2010) emphasized the need to cope better with nutrient limitations in the carbon-centric view dominating tree physiology over the past decades. Remobilization processes enable plants to reuse the nutrients and therefore play an important role for maintaining tree growth in infertile soils making them less dependant on current nutrient uptake. The vast majority of studies dealing with nutrient remobilizations in forest have been conducted throughout leaf senescence (e.g. Nambiar and Fife 1991; Aerts and Chapin 2000). The amounts of N, phosphorus (P) and potassium (K) remobilized from the leaves of 4 evergreen tree species in Australia were strongly positively correlated with their content in fully expanded young leaves (Fife et al. 2008), which was consistent with a general pattern of source-driven N remobilizations within trees (Millard and Grelet 2010). However, remobilizations in tree compartments other than leaves have still been little investigated in the field. Most of the studies on mature trees focused on carbon (C) and N remobilizations using the possibility to track C and N stable isotopes after pulse labeling (e.g. Millard and Grelet 2010; El Zein et al. 2011; Epron et al. 2012). Nitrogen is the most limiting nutrient for tree growth in many forests of the Northern hemisphere (Rennenberg et al. 2009). However, tree growth in highly weathered tropical soils is commonly more limited by P (Vitousek et al. 2010) and K (Laclau et al. 2009; Wright et al. 2011; Santiago et al. 2012) than by N. Studies using stable isotopes other than
15

N to gain insight into

nutrient remobilizations within ligneous tree components are scarce and, to our knowledge, have only been carried out for seedlings (Proe et al. 2000; Weatherall et al. 2006). The lack of cheap stable isotopes of P, K, calcium (Ca) and magnesium (Mg) for field-use as well as a smaller scientific community in tropical regions than in

4 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 Most of tropical Eucalyptus plantations are established on highly weathered soils and sustainable yields are largely dependent on fertilization regimes (Gonalves et al. 2008; Laclau et al. 2010). In Brazil, large amounts of fertilizers applied the first two years after planting make it possible to reach gross primary productivities > 4000 g C m-2 yr-1 (Ryan et al. 2010), among the highest for world forests (Luyssaert et al. 2007). Fertilizer applications are concentrated the first year after planting and remobilization processes play a major role to satisfy the N, P and K requirements after canopy closure in tropical Remobilizations within stem wood contribute to reducing nutrient concentration in the boles harvested and therefore to balance the input-output of nutrients in forest soils when the length of the rotation increases (Ranger and Turpault 1999; Ranger et al. 2002). A budget approach in annual rings was widely used in the 80s and 90s to estimate nutrient remobilizations within stem wood over forest rotations in temperate and boreal regions. Large remobilizations of N, P, K and to a lesser extent, Mg, throughout wood ageing have been shown for many tree species (e.g. Colin-Belgrand et al.1996; Helmisaari and Siltala 1989; Hingston et al. 1979; Lim and Cousens 1986). However, nutrient remobilization within stem wood of tropical tree species with continuous growth along the year is poorly known. A chronosequence approach in fastgrowing Eucalyptus plantations in the Congo showed that the mobility of N, P, K, Ca and Mg in the stem wood was similar to that in deciduous species (Laclau et al. 2001; Saint-Andr et al. 2002). However, the seasonal patterns and the influence of soil fertility on nutrient remobilizations within stem wood were not investigated. industrialized countries probably has led to a shortage of information on remobilizations of nutrients others than N within tree compartments in the field.

5 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 MATERIAL AND METHODS Study area The study was carried out at the Itatinga Experimental Station (2310 S and 48 40 W). The mean annual rainfall over the 15 years before our study was 1360 mm and the mean annual temperature was 20C, with a seasonal cold period from June to September. The experiment was located on a hilltop (slope < 3%) at an altitude of 850 m. The soils were very deep Ferralsols (> 15 m) developed on Cretaceous sandstone, Marlia formation, Bauru group, with a clay content ranging from 14% in the A1 horizon to 23% in deep soil layers. The mineralogy was dominated by quartz, kaolonite and oxyhydroxides, with acidic soil layers (pH between 4.5 and 5) containing very We put forward the hypotheses that: 1) source-driven processes in Eucalyptus trees increase the remobilizations of nutrients applied with fertilizers per unit of stem wood biomass produced, and 2) Eucalyptus trees remobilize large amounts of Na stored in the stem wood in substitution for K in K-deficient soils when the availability of Na increases. We used a mass balance approach in annual rings to gain insight into the role of the stem wood for the storage of nutrients throughout the development of Eucalyptus trees. Eucalyptus plantations (Laclau et al. 2003). Recent studies have shown that a small supply of NaCl in Eucalyptus grandis Hill. ex Maiden stands established on K-depleted soils enhanced the stem wood biomass by 55% at the harvest relative to control plots without NaCl addition (Ameida et al.,2010; Epron et al. 2012). The low cost of NaCl in comparison to purified KCl fertilizers might lead to a large scale application of a mixture between KCl and NaCl in tropical eucalypt plantations (Almeida et al. 2010).

6 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 Experimental design Eucalyptus grandis seedlings genetically improved by the Suzano Company (half-sib seeds) were planted in April 2004 between the stumps of the previous rotation (spacing 2 m x 3 m). A complete randomized block design was installed with 6 treatments and 4 blocks with individual plots of 9 * 9 trees. A completed description of the experiment is given by Almeida et al. (2010). Our study was carried out in 3 treatments and 3 blocks : (i) C, Control with no K and no Na input; (ii) +K, 3 kmol K ha-1 (116 kg K ha-1) applied as KCl fertilizer (a similar amount is applied in commercial plantations of the region) and (iii) +Na, 3 kmol Na ha-1 (68.5 kg Na ha-1) applied as NaCl fertilizer. A third of the total amount was applied at planting (buried at 20 cm from the seedlings), then at 6 months (broadcast beneath the crowns) and 12 months of age (broadcast over the entire area). All treatments received the same basic fertilization regime (except K and Na), The experiment was set up in a Eucalyptus saligna (Sm.) stand conducted as a coppice, without any fertilizer application from 1940 to 1997. Herbicide was applied on the stumps to prevent regrowth and E. saligna seedlings were planted in 1998 with a low fertilizer supply (30 kg N ha-1, 9 kg P ha-1, 8 kg K ha-1). High levels of nutrient exports with the boles, without fertilization from 1940 to 1998, made the area suitable to expect a eucalypt response to fertilizer inputs. The E. saligna stand was harvested at age of 6 years (February 2004) and the stumps were devitalized using an application of glyphosate. Boles were removed from the site and harvesting residues were uniformly distributed. small amounts of available nutrients (sum of base cations < 0.3 mmolc kg-1, between the depths of 5 cm and 6 m) (Laclau et al. 2010).

7 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 Taper functions were used for estimating stem profiles under-bark at 1, 2 and 3 years after planting. The circumference of each tree sampled destructively (32 trees per Tree sampling Tree height and circumference at 1.3 m above-ground (C1.3) were measured every 12 months in the inner plots (excluding 2 buffer rows) the first 4 years after planting. Destructive samplings of biomass and nutrient contents were carried out at 1, 2, 3 and 4 years after planting in one block of the experiment. At each stand age, the range of basal areas in each treatment was divided in 4 classes of similar extent and 2 trees were sampled in each class. Disks of wood were taken at the ground level and every 3 meters for each selected tree. Chemical analyses were conducted on a composite sample of stem wood (proportional to the dry matter of wood at all the sampled heights) for the 96 trees sampled (8 trees x 3 treatments x 4 ages) and allometric relationships were established to estimate the biomass and nutrient contents of stem wood at each age (see Almeida et al. 2010 for a detailed description). For half of the sampled trees (1 tree per basal area class at each age in each treatment), virtual annual rings were positioned on all the disks of wood sampled. The continuous growth throughout the year in tropical eucalypt plantations prevent from distinguishing annual rings. The methodology described by Laclau et al. (2001) to estimate annual remobilizations within stem wood over a full rotation in Eucalyptus plantations was adapted here. The first step was to rebuild the cambial growth of a tree from stem profiles. with an addition, the first year after planting, of 120 kg N ha-1, 35 kg P ha-1, micronutrients, and 2 t ha-1 of dolomitic lime, not limiting tree growth at the study site (Gonalves et al. 2008).

8 170 171 172 treatment up to 4 years of age) was measured under-bark every meter, up to a diameter of 2 cm. To predict the diameter under-bark (dz) at height z, models were adjusted (Newnham 1992):
P z ( 3 ) P 2H ) (P 1 + P2 e

173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193

dz H z = d1.3 H 1.3

+.

(1)

where follows a normal distribution, d1.3 and H are respectively the diameter underbark at 1.3 m above-ground (expressed in centimetres) and the total height of the tree (in meters). The parameters P1, P2 and P3 were adjusted to the measurements of diameter under-bark for each stand age. Root mean square errors of the models were low and residue repartitions were not biased for all the sampled trees.

Annual measurements of C1.3 and H for all the sampled trees, combined with treatmentspecific taper functions, made it possible to predict the diameter under-bark at 1, 2 and 3 years of age, whatever the height on the stem. Virtual annual rings were thus positioned on each disk of wood sampled. Each annual ring boundary was delineated on the disk using two criteria: i) the mean radius of the ring (measured in eight directions) was the value predicted by the taper function, and ii) the boundaries were parallel to growth rings visible to the naked eye. Rings are commonly observed in tropical Eucalyptus species but the number of rings may be different from tree age (Sette Jr et al. 2010).

Wood density and chemical analyses

The wood of each annual ring was separated in all the disks and dried at 65C until constant weight. Half of each sample was used to determine wood density and the other half was ground and homogenised for chemical analyses. Wood density was determined for each annual ring at each tree height sampled from the maximum moisture content
8

9 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208
209 210 211 212 213 214 215 216 217 218
Calculations

method adapted to small wood samples (Smith 1954). Chemical analyses were made in Brazil for one composite sample of stem wood per tree for the 96 trees sampled. After digestion in nitric and perchloric acids, Ca and Mg were determined by atomic absorption spectrophotometry (B462, Micronal, Brazil) and K and Na by flame emission spectrophotometry (Malavolta et al. 1989). For half of the sampled trees, chemical analyses were performed in France individually for each ring per level. Phosphorus, K, Ca, Mg and Na were determined using an ICP sequential spectrophotometer (JY 24) after digestion by hydrofluoric acid and double calcination. Control quality procedures were used in the two laboratories and samples were analysed in duplicate for inter-calibration.

Dynamics of nutrient accumulation within stem wood Stem wood biomass and nutrient contents were estimated from the 8 trees sampled in each treatment at each age using the model:
Yi = a + b( Di H i ) j + i where Yi is the biomass or the nutrient content of the stem wood of tree i, Di is the diameter at breast height of tree i, Hi is the height of tree i, a, b and c are the parameters to be estimated and i is the residual error not explained by the model. As age was found to significantly affect this relationship (Saint-Andr et al. 2005), the equations were fitted by treatment for each age. Fitting was performed using PROC NLP of the SAS software and maximum likelihood estimations. To test treatment effects, comparisons between models were performed using the Akaike information criterion.
2 c

10 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 The mean nutrient concentration (Ctree) within ring i in a given sampled tree was calculated using the equation: The amount of mineral M, Mz, [i-1,i], contained in the wood formed between age (i-1) and age i at height z, in a disk of thickness 1 cm, was calculated using the equation:
M z ,[i 1,1] = C z ,[i 1,i ] S z ,[i 1,i ] d z ,[i 1,i ]

Mean nutrient concentration per ring in the 4 trees per treatment sampled at each age The area of each annual ring was calculated considering that all the rings were circular:
2 2 S z,[i1, i] = (r z, r ). i z, i1

(2)

where Sz.[i-1. i] is the area of the ring corresponding to the wood formed between age (i-1) and age i at height z, and where rz, i-1 and rz. i are the radius under-bark of the stem at height z predicted by the taper functions (equation 1) at age (i-1) and age i, respectively.

(3)

where Cz,[i-1,i] and dz,[i-1,i] are the mineral concentration and the density of the wood formed between age (i-1) and age i at height z, respectively.

M
234

z ,[i 1,1]

(Ctree )i

z =0

S
z =0

z =n

(4)

z ,[i 1,i ]

d z ,[i 1,i ]

235 236 237 238 239 240

where ring i was the ring formed between age (i-1) years and age i years, and n the number of heights sampled in the tree.

Estimation of nutrient contents in annual rings for the whole stand Mean wood density in ring i at for the whole stand was estimated at each age from the equation:

10

11

241

d i = p
p =0

S
z =0

i,z, p n

d i,z, p
(5)

Si,z, p
z =0

242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262

where Si,p,z and di,p,z are the area and the wood density of ring i at height z for tree p, and p is the proportion of total stand basal area represented by the basal area class of tree p.

Wood biomass in each annual ring was estimated for the whole stand using equation (6) for internal rings and equation (7) for the external ring of the trunk.

For an internal ring i in a stand of age a > i:

Bi , a = Bi , 0 d i ,a d i,0

(6)

where Bi,0 is the biomass of ring i the year of its formation, di,a and di,0 are the mean wood densities in ring i estimated from equation (5) the year of wood formation and at a years after planting, respectively.

For the external ring i in a tree of age a (a = i), we used the equation:
k =i 1

Bi , a = Btot ,a

B
k =1

k ,a

(7)

where Btot,a is the total stem wood biomass of the stand at age a estimated applying allometric equations to the inventory, and Bk,a is the biomass of ring k calculated with equation (6).

The mean nutrient concentration within ring i in the stand (Cstand)i was estimated using the equation:

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12

263 264 265 266 267 268

(C s tan d )i = p (Ctree ) p,i .

p =1

(8)

where (Ctree)p,i is the mean nutrient concentration within ring i in the tree p.

Nutrient contents in a given ring per hectare (Ni) were thus estimated multiplying the wood mass of the ring estimated with equations (6) and (7) by the mean concentrations in the ring estimated with equation (8). The equation used was: (C s tan d ) i Bi ,a ,l
v

269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 284

Ni =

l =1

(9)

where Bi,a,l is the mass of ring i in a tree l of age a, v is the number of trees inventoried and A the area of the studied plot.

Nutrient remobilizations at the stand level Annual remobilizations were calculated stepwise between two successive ages. Nutrient remobilizations into the i ring from (a-1) to a years after planting, (Ri.[a-1. a]) were calculated with the equation:
Ri [a 1,a ] = N i ,a 1 N i ,a

(10)

Total remobilization in stem wood between the successive ages (a-1) and a (Rtot [a-1. a]) was calculated by adding the nutrient remobilizations in all the rings initiated before age (a-1) with the equation:

Rtot,[a 1,a] =

R
i =1

a 1

i,[a 1, a]

(11)

Nutrient remobilization efficiency Nutrient remobilization efficiency was assessed for the wood produced the first 2 years

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13 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309
Statistical analyses

after planting because heartwood stands only in the two first rings in 4-year-old trees. The equation used was:
E N ,i ,t = 100 C i ,i C i , 4 ( d i , 4 d i , i ) C i ,i

(12)

where EN,i, t is the remobilization efficiency of nutrient N in the ring produced the ith year after planting (i = 1 or 2) in tree t, Ci,4 is the concentration of nutrient N in ring i of tree t at age 4 years, and di,4 is the wood density in ring i of tree t at age 4 years. Equation (12) was used for the 4 trees sampled at age 4 years in each treatment for annual ring determinations. We considered that Ci,i and di,i were the nutrient concentration and the wood density, respectively, in ring i of the tree sampled at age i years in the same treatment for the same basal area class.

Differences in nutrient concentrations between tree ages, tree social status (basal area class) and treatments were tested using the MIXED procedure of the SAS software. Ring cambial age (number of years since ring formation), tree social status and treatment were considered as fixed factors. Annual rings were considered as random factor. Observations were assumed to be uncorrelated among the sampled trees because they were cut far from each other. The probability level used to determine significance was P < 0.05. When differences were significant, the means were compared with the Tukey-Kramer multiple comparison tests using the Lsmeans / Pdiff option. Two-way ANOVAs were used to test the effects of treatments and tree social status on the remobilization efficiencies of each nutrient in an individual ring. The GLM procedure of the SAS 9.2 software package was used (SAS Inc., Cary, NC, USA). A residual analysis was performed to check whether the residuals met the assumptions of the ANOVA and, if necessary, raw data were log- or sqrt- transformed so that residuals 13

14 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334
RESULTS Dynamics of biomass and nutrient accumulation in stem wood

were homoscedastic and normally distributed. When significant differences were detected between treatment levels, the Tukey multiple range test was used to compare treatment means.

Potassium and Na additions significantly increased the stem wood biomass the first 4 years after planting (Fig. 1). At 4 years of age, it was higher by 116% and 51% in treatments +K and +Na, respectively, than in the C treatment. The biomass of the rings produced the first, second, third and fourth years after planting amounted to 2-3%, 2428%, 32-34% and 36-41% of the stem wood biomass at age 4 years in the three treatments. Nutrient contents within stem wood were driven by both biomass accumulation and changes in nutrient concentrations throughout the study period. A low tree growth in the C treatment led to a lower accumulation of P, K, Ca, Mg and Na in stem wood than in treatments +Na and +K. Whilst P, Ca and Mg contents within stem wood were mainly driven by the accumulation of biomass in the 3 treatments, K and Na additions the first year after planting largely influenced their content within stem wood up to 4 years of age. A similar K accumulation in treatments C and +Na, despite a stem wood biomass in +Na 51% larger than in C at 4 years after planting, suggested that the enhancement in tree growth after Na addition was not due to a higher K uptake in the soil. Sodium addition the first year after planting led to an accumulation of Na within stem wood about twice as high in treatment +Na, as in the C and +K treatments at 4 years of age. The amounts of K and Na within stem wood decreased by 8-24%, from 3 to 4 years after planting in the 3 treatments (except for Na in treatment C), although the biomass of this compartment increased by about 50%. This result suggested intense

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15 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 The concentration of Na in the outer ring was about twice as low in the +K treatment as in treatment C, whatever the tree age, and the decrease in concentrations of Na throughout ring ageing was less pronounced in the +K treatment than in treatments C and +Na (Fig. 2). A sharp decrease in K concentrations with ring ageing irrespective of the treatment suggested that K was strongly remobilized in our K-deficient soil, even when the availability of Na rose. The social status of the trees (dominated or dominant
Concentrations of K, Na, P, Ca and Mg within annual rings

remobilizations of those nutrients in the stem wood at the end of the study period.

A general pattern of decrease in concentrations of K, Na and P from the outer to the inner rings, whatever the tree age, showed that these nutrients were found in the most physiologically active tissues (Fig. 2). Nutrient withdrawals were higher the first two years after the formation of the ring than thereafter. Potassium and Na additions significantly increased the concentrations of those elements within annual rings (Table 1 and Fig 2). The concentrations of Ca and Mg in annual rings were also significantly influenced, with higher concentrations at most ring cambial ages in the C treatment than in treatments +K and +Na. The interaction between ring cambial age and treatment was significant for the concentrations of K, Na and Ca. This pattern for K and Na resulted from a sharper decrease in concentration with ring ageing for the trees fertilized with these elements than in the other treatments (Fig. 2). In the case of Ca, the interaction resulted from a slight decrease in concentrations after ring formation in treatments +K and +Na whereas the concentrations of this element changed little throughout ring ageing in the C treatment (a trend towards an accumulation was found in the ring produced the first year after planting).

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16 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 Remobilization efficiencies in the rings produced the first two years after planting were not significantly different between treatments, except for P in the inner ring (Table 2). The effects of tree social status on remobilization efficiencies were not significant
Nutrient contents and remobilizations in annual rings

in the stand) did not significantly influence the concentrations of K, Na, P, Ca and Mg in annual rings over the study period (Table 1). Interactions between the social status and the age of the sampled trees were not significant as well as interactions between tree social status and tree age, whatever the nutrient.

The amounts of nutrients in annual rings were largely driven by the mass of the ring (Fig. 3). Even though large changes in nutrient concentrations were found in the wood produced the first year after planting, the contribution of this ring in annual remobilizations within stem wood was minor from 2 years after planting onwards. The highest mineral contents were found in the outer rings at each age. Outer rings had both the largest biomass and the highest nutrient concentrations (except for Ca). Even though changes in Na concentrations throughout ring ageing in treatment +K were low in comparison with the C treatment, the much larger stem wood biomass in +K led to similar amounts of Na in annual rings as in the control treatment throughout the study period. The amounts of K in annual rings were little influenced by Na application over the first 4 years after planting. The highest accumulation of K and Na in the stem wood of the +K and +Na treatments, respectively, was mainly a result of high K and Na contents in the 2 outer rings (Fig. 1). The highest accumulation of P, Ca and Mg in the stem wood of the +K treatment at each age was also mainly localized in the 2 outer rings.

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17 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409
DISCUSSION Nutrient concentrations in annual rings

whatever the nutrient and the annual ring. Mean remobilization efficiencies across treatments in the 2 inner rings were 83%, 72%, 87%, 4% and 51% for K, Na, P, Ca and Mg, respectively.

Annual remobilizations of K, Na, P, Ca and Mg within stem wood increased throughout stand development, irrespective of the treatment (except for Mg in treatment +K). Among the studied nutrients, the highest remobilizations occurred for K (Table 3). The annual amounts of K remobilized in the stem wood were 4.5, 15.7 and 1.7 times higher for trees in the +K treatments than in treatment C, the second, third and fourth year after planting (1, 2 and 3 years after fertilizer addition), respectively, for a stem wood biomass production about 2-fold larger. Annual K remobilizations over the study period were of the same order of magnitude in the C treatment and in Na-fertilized trees. Whilst Na was not remobilized in well K-supplied trees the second and the third years after planting, high remobilizations occurred in treatment +Na. Annual Na remobilizations from 1 to 4 years after planting in treatment +Na were 2-3 times higher than in the C treatment. The amount of Na remobilized in annual rings was 15% higher in +Na than in +K the 4th year after planting despite a 34% smaller stem wood biomass production. In the +Na treatment, the amounts of K and Na remobilized within the stem wood were of the same order of magnitude up to 4 years after planting. Although stem wood biomass at age 4 years was 2.3-fold larger in +K than in C, the annual remobilizations of P, Ca, Mg the 4th year after planting were only higher in +K by 25%, 49% and 17%, respectively.

17

18 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 The dynamics of nutrient concentrations in annual rings commonly described for tree species were not modified by fertilizer addition in our study. Whilst, the concentrations Although annual rings cannot be detected visually in tropical Eucalyptus grandis trees, our method combining annual inventories with stem profile equations and intensive sampling of disks along the trunk in 4 trees per treatment and per age provided estimates of nutrient contents in the stands of the same magnitude as sampling 8 trees per age in each treatment. Consistent changes in concentrations of mobile nutrients within annual rings throughout stand development in each treatment confirmed that the boundaries of each ring were correctly delimited. The non-significant influence of the tree social status on nutrient concentrations in annual rings supported our simple upscaling approach to estimate mean nutrient concentrations in annual rings for the whole stand. Budgets of nutrients in tree compartments are, however, dependent on the timing of sampling and this method is usually considered less accurate than isotopic approaches to estimate nutrient remobilizations (Millard and Grelet 2010). Total retranslocations might have been underestimated in our study since the continuous growth of tropical Eucalyptus trees might have led to several storage/remobilization phases within annual rings along the year. However, nutrient budgets can be a suitable approach to quantify the remobilization of nutrients from ligneous tree components in the field when stable isotopes cannot be used (Milla et al. 2005). Nutrient concentrations within tree rings were so different between treatments in our study that the budgets clearly showed a strong effect of K and Na additions on nutrient remobilizations. Further studies based on intensive sampling of xylem sap would be useful to gain insight into the amounts and the types of compounds translocated seasonally from the stem and the roots in plantation forests (Pfausch et al. 2009).

18

19 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459
Source-driven remobilizations within stem wood

of P and K decreased sharply over ring ageing, the mobility of Ca was low and Mg was intermediate, as reported for other Eucalyptus species (Turner and Lambert 1983; Grove et al. 1996; Laclau et al. 2001; Saint-Andr et al. 2002). A similar pattern was found in Picea abies (Dambrine et al.. 1991), Castanea sativa (Colin-Belgrand et al., 1996), Pinus sylvestris L. (Helmisaari and Siltala 1989; Finr and Kaunisto 2000), Quercus robur L. (Pennincks et al., 2001) and Pinus pinaster (Augusto et al., 2008). Although radial variations in wood mineral concentrations are highly species- and elementspecific (Penninks et al. 2001), the concentrations of N, P and K are, in general, higher in the sapwood than in inner rings as a result of their metabolic role in living cells (Meerts 2002). Microscopic, molecular and biophysical techniques showed that K is mainly required for cell expansion in cambial cells, whereas Ca seems to be essential for cell division and cell wall strengthening (Fromm 2010). Changes in radial concentrations of K, Na, P, Ca and Mg throughout stem growth seem, therefore, to reflect both the role of these elements in cambial activity and their mobility in xylem cells.

Nutrient remobilizations in senescent leaves have been extensively studied and their adaptative significance is well documented (e.g. Aerts and Chapin III 2000). Remobilization processes enable plants to reuse the nutrients and therefore play an important role for maintaining tree growth in infertile soils making them less dependant on current nutrient uptake. Large ranges of remobilization rates from senescent leaves have been reported for N and P, with median values around 50% for plant species in natural ecosystems (Aerts and Chapin III 2000). Remobilization efficiencies of K, Na and P within stem wood in our study were at the upper range of values reported

19

20 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 In agreement with our first hypothesis, the dynamics of nutrient concentrations within stem wood showed that remobilizations were mainly source-driven. This feature was particularly clear for Na. Remobilizations of Na were estimated at 11, 205 and 312 mol ha-1 in treatment +Na the second, third and fourth year after planting, respectively, whereas they only amounted to 1, -10 and 271 mol ha-1 in treatment +K (Table 3). The 43% larger stem wood biomass in treatment +K than in +Na at age 4 years even led to a much stronger nutrient sink in K-supplied trees. The amounts of K remobilized in annual rings of K-deficient trees were close in the +Na and C treatments in our study throughout leaf senescence in tree species (e.g. Fife et al. 2008; Kozovits et al. 2007; Saur et al. 2000). Even though N remobilizations are seasonally programmed in temperate and boreal tree species (Millard and Grelet 2010), the continuous growth along the year of E. grandis trees did not prevent it from large remobilizations of K, Na and P in the stem wood. The highest nutrient availability in the soils under fast-growing Eucalyptus plantations occur the first year after planting as a result of large fertilizer inputs combined with a high amount of nutrients released via organic matter decomposition and a relatively low nutrient uptake by trees the first months after planting (Laclau et al. 2010). The sharp decrease in K, P and Mg concentrations in the outer ring from 1 to 3 years after planting in the +K treatment (Fig. 2) suggests that the sapwood in E. grandis trees has a capacity to accumulate nutrients when their availability is high, far beyond the necessity required for cambial activity and xylem cell development. The capacity of Eucalyptus trees to store nutrients within stem wood for a further use when the demand for growth is much higher is likely to contribute to preventing nutrient losses by deep drainage in forests established on sandy soils with high hydraulic conductivities.

20

21 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509
Remobilizations of Na within stem wood

despite a 51% larger stem wood biomass at age 4 years in +Na, leading to a much stronger K sink. Our results suggest that K and Na remobilizations in stem wood follow the general tendency found for N in both coniferous and deciduous species whose remobilizations depend upon the amount of nutrients in store, not the amount of new growth or current uptake rate (Carswell et al. 2003; Millard and Grelet 2010). However, information for nutrients other than N is scarce and suggests that the effect of nutrient supply on remobilizations may not always be the same for all the nutrients. Remobilizations of K and Mg were, like that of N, independent of current nutrient supply in Picea sitchensis (Bong.) Carr. seedlings labelled with
15

N,

41

K and

26

Mg

(Weatherall et al. 2006). Nevertheless, another study using the same isotopes in Pinus sylvestris L. seedlings showed a different behaviour between those nutrients: whilst current nutrient supply had no significant effect on the amount of N or Mg remobilized to new tissues, K remobilization was lower in seedlings growing on sand culture with a reduced nutrient supply (Proe et al. 2000).

In agreement with our second hypothesis, large amounts of Na were remobilized in the stemwood of Na-supplied trees in our K-depleted soil. Epron et al. (2012) showed that the addition of 4.5 kmol ha-1 of NaCl increased the stem wood biomass of E. grandis trees by 130% at harvest in our experiment. A growing body of evidence led Subbarao et al. (2003) to consider Na as a functional nutrient that can be important in the physiology of numerous glycophyte species under K starvation conditions. Similar dynamics within annual rings for Na, as for K in our study, as well a strong response to NaCl addition in biomass production, suggest a substitution of K by Na in living wood cells for certain physiological functions. The osmotic role of K for the expansion of

21

22 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534
REFERENCES ACKNOWLEDGEMENTS

xylem cell is well established (Fromm 2010) and further studies are needed to assess whether this function can be fulfilled by Na, as shown by Battie-Laclau et al. (2012) for the maintenance of osmotic potential and cell turgor in leaves of K-starved E. grandis trees. Potassium remobilizations in the branches of evergreen Mediterranean species also appeared to be related to osmotic requirements (Milla et al. 2005).

In conclusion, the annual remobilizations of K, Na, P, Ca and Mg within the stem wood of E. grandis trees were mainly source-driven the first four years after planting. High remobilizations of Na on a K-depleted soil were likely to contribute to the enhancement of stem wood production by about 50%, via a reduction in K requirements for the development of the trees. Further studies are needed to gain insight into the physiological mechanisms responsible for the positive effects of low NaCl additions on the growth of Eucalyptus trees in highly weathered soils. The function of Na in the biological cycle of forest ecosystems would deserve further attention, since the availability of this element might contribute to driving tree growth in K-depleted tropical soils subjected to high marine aerosol input.

We are particularly grateful to Eder Araujo da Silva (www.floragroapoio.com.br) for his contribution to this study. We thank FAPESP and CIRAD for their financial support.

Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597608.

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26 610 611 612 613 614 615 616 617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 Laclau J-P, Deleporte P, Ranger J, Bouillet J-P, Kazotti G (2003) Nutrient dynamics throughout the rotation of Eucalyptus clonal stands in Congo. Ann Bot 91:879-892 Laclau J-P, Ranger J, Deleporte P, Nouvellon Y, Saint-Andr L, Marlet S, Bouillet J-P (2005) Nutrient cycling in a clonal stand of Eucalyptus and an adjacent savanna ecosystem in Congo: input-output budgets and consequences for the sustainability of the plantations. For Ecol Manage 210: 375-391 Laclau J-P, Almeida JCR, Gonalves JLM, Saint-Andr L, Ventura M, Ranger J, Moreira MR, Nouvellon Y (2009) Influence of nitrogen and potassium fertilization on leaf lifespan and allocation of above-ground growth in Eucalyptus plantations. Tree Physiol 29:111124 Laclau J-P, Ranger J, Gonalves JLM, Maqure V, Krusche AV, M'Bou AT, Nouvellon Y, Saint-Andr L, Bouillet J-P, Piccolo MC, Deleporte P (2010) Biogeochemical cycles of nutrients in tropical Eucalyptus plantations: Main features shown by intensive monitoring in Congo and Brazil. For Ecol Manage 259: 1771-1785 Lim MT, Cousens JE (1986). The internal transfer of nutrients in a Scots pine stand. 2. The patterns of transfer and the effects of nitrogen availability. Forestry 59: 17-27 Liu X, Xu H, Berninger F, Luukkanen O, Li C (2004) Nutrient distribution in Picea likiangensis trees growing in a plantation in west Sichuan. Southwest China. Silva Fennica 38: 235242 Luyssaert S, Inglima I et al (2007). CO2 balance of boreal, temperate, and tropical forests derived from a global database. Glob Change Biol 13:25092537 Matson JL, Mayville EA, Bielecki J, Smalls Y, Eckholdt CS (2002). Tardive dyskinesia associated with metoclopramide in persons with developmental disabilities. Research in Developmental Disabilities 23: 224233 McClenahen JR, Vimmerstedt JP, Scherzer AJ (1989) Elemental concentrations in tree

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29 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 29 Sette Jr CR, Tomazello F M, Dias CTS, Laclau, J-P (2010) Crescimento em dimetro do tronco das rvores de Eucalyptus grandis W. Hill. EX. Maiden e relao com as variveis climticas e fertilizao mineral. Revista rvore 34:979-990 Smith DM (1954) Maximum moisture content method for determining specific gravity of small wood samples. U.S. Forest Products Laboratory Report 2014:1-8 Staaf H (1982) Plant nutrient changes in beech leaves during senescence as influenced by site characteristics. Oecologia 3:161-170 Subbarao G, Ito O, Berry W, Wheeler R (2003) Sodium: a functional plant nutrient. Plant Science 22:391-416 Turner J, Lambert MJ (1983). Nutrient cycling within a 27-year-old Eucalyptus grandis plantation in New South Wales. For Ecol Manage 6: 155-168 Van Bel AJE (1990) Xylem-Phloem exchange va the rays: the undervalued route of transport. J Exp Bot 41: 631-644 Van Den DR (1984) Relationship between spacing and nitrogen fertilization of seedlings in the nursery. seedling mineral nutrition. and outplanting performance. Can J For Res 14:43 l-436 Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial P limitation: mechanisms, implications, and N-P interactions. Ecological Applications 20: 5-15 Wright SJ et al (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92: 1616-1625 Yanai RD, Battles JJ, Richardson AD, Blodgett CA, Wood DM, Rastetter EB (2010) Estimating uncertainty in ecosystem budget calculations. Ecosystems 13: 239248 Zas R, Serrada R (2003) Foliar nutrient status and nutritional relationships of young Pinus radiata D. Don plantations in north-west Spain. For Ecol Manage 174: 167176

30 707 708 709 710 711 712 713 714 715 716 717 718 719 720 Fig. 3. Changes in K, Na, P, Ca and Mg contents within annual rings over the first 4 years after planting in treatments C (a, b, c, d, e, respectively), +K (f, g, h, i, j, respectively), and +Na (k, l, m, n, o, respectively). Fig. 2. Changes in concentrations of K, Na, P, Ca and Mg within annual rings over the first 4 years after planting in treatments C (a, b, c, d, e, respectively), +K (f, g, h, i, j, respectively), and +Na (k, l, m, n, o, respectively). Fig. 1. Dynamics of biomass, phosphorus (P), potassium (K), sodium (Na), calcium (Ca) and magnesium (Mg) accumulation within stem wood the first 4 years after planting, estimated sampling 8 trees per treatment at each age. Least significant differences between treatments (P < 0.05) are indicated at each age.
Figure captions

30

Figure 1

100

250
-1

Stem wood biomass (Mg ha )

LSD 80

P accumulation (mol ha )

-1

LSD 200

60

150

40

100

20 Control +K +Na

50

0 0 1400 1 2 3 4

0 0 1000 1 2 3 4

1200 1000 800 600 400 200 0 0 1000 1 2 3 4

Na accumulation (mol ha )

K accumulation (mol ha )

-1

-1

LSD

LSD 800

600

400

200

0 0 800
-1

-1

LSD 800

Mg accumulation (mol ha )

Ca accumulation (mol ha )

LSD 600

600

400

400

200

200

0 0 1 2 3 4 Stand age (years)

0 0 1 2 3 4 Stand age (years)

Fig. 1. Dynamics of biomass, phosphorus (P), potassium (K), sodium (Na), calcium (Ca) and magnesium (Mg) accumulation within stem wood the first 4 years after planting, estimated sampling 8 trees per treatment at each age. Least significant differences between treatments (P < 0.05) are indicated at each age.

Figure 2

C
2.5 K concentration (g kg )
-1

+K
2.5
Ring 1 Ring 2 Ring 3 Ring 4

+Na
2.5

a)

f)
2.0 1.5 1.0 0.5 0.0 2.0 1.5 1.0 0.5 0.0 0 0.8 1 2 3 4 0.8 0

k)

2.0 1.5 1.0 0.5 0.0

0 1 2 3

0.8 Na concentration (g kg )
-1

b)

g)

l)

0.6

0.6

0.6

0.4

0.4

0.4

0.2

0.2

0.2

0.0 0 0.2 P concentration (g kg ) 1 2 3 4

0.0 0 0.2 1 2 3 4

0.0 0 0.2 1 2 3 4

c)

h)

m)

-1

0.1

0.1

0.1

0.0 0 1.5 Ca concentration (g kg )

-1

0.0 1 2 3 4 1.5 0 1 2 3 4

0.0 0 1.5 1 2 3 4

d)

i)
1.0 1.0

n)

1.0

0.5

0.5

0.5

0.0 0 0.5 Mg concentration (g kg )

-1

0.0 1 2 3 4 0.5 0.4 0.3 0.2 0.1 0.0 0 1 2 3 4 0 1 2 3 4 0 1 2 3 4

0.0 0 0.5 0.4 0.3 0.2 0.1 0.0 0 1 2 3 4 1 2 3 4

e)

j)

o)

0.4 0.3 0.2 0.1 0.0

Stand age (years)

Stand age (years)

Stand age (years)

Fig. 2. Changes in concentrations of K, Na, P, Ca and Mg within annual rings over the first 4 years after planting in treatments C (a, b, c, d, e, respectively), +K (f, g, h, i, j, respectively), and +Na (k, l, m, n, o, respectively).

Figure 3

1000 K content (mol ha ) 800 600 400 200 0

-1

C
a)
Ring 1 Ring 2 Ring 3 Ring 4

1000 800 600 400 200 0

+K
f)

1000 800 600 400 200 0

+Na
k)

0 500 Na content (mol ha )

-1

4 500 400 300 200 100 0

4 500 400 300 200 100 0

b)

g)

l)

400 300 200 100 0 0 100 1 2 3 4

0 100

4 100

P content (mol ha )

c)

-1

h)
80 60 40 20 0 80 60 40 20 0 0 300 1 2 3 4 300

m)

80 60 40 20 0 0 300 1 2 3 4

Ca content (mol ha )

-1

d)
200 200

i)

n)

200

100

100

100

0 0 300 Mg content (mol ha )

-1

0 1 2 3 4 300 0 1 2 3 4

0 0 300 1 2 3 4

e)

j)
200

o)

200

200

100

100

100

0 0 1 2 3 4

0 0 1 2 3 4

0 0 1 2 3 4

Stand age (months)

Stand age (months)

Stand age (months)

Fig. 3. Changes in K, Na, P, Ca and Mg contents within annual rings over the first 4 years after planting in treatments C (a, b, c, d, e, respectively), +K (f, g, h, i, j, respectively), and +Na (k, l, m, n, o, respectively).

Table 1

Table 1. Influence of ring cambial age, treatment and social status of sampled trees on the concentrations of K, Na, P, Ca and Mg in annual stem wood rings produced the first 4 years after planting in Eucalyptus grandis stands. Significant values (P < 0.05) are indicated in bold.
Nutrient Fixed factors Ring cambial age Treatment Social status Cambial age * Treatment Cambial age * Social status Treatment * Social status K dF
3 2 3 6 6 9

Na P
<.0001 0.004 0.5436 0.002 0.9339 0.325

P P F
102.7 2.6 0.2 0.3 0.6 0.4

Ca P
<.0001 0.0767 0.9053 0.939 0.7209 0.9491

F
149.5 5.9 0.7 3.8 0.3 1.2

F
67.1 57.6 1.2 6.8 1.1 0.5

F
12.3 18.6 2.2 4.2 0.4 0.9

P
<.0001 <.0001 0.0877 0.009 0.9021 0.4922

F
43.6 11.0 1.7 1.6 1.1 0.4

Mg P
<.0001 <.0001 0.1761 0.1638 0.3453 0.9461

<.0001 <.0001 0.3022 <.0001 0.3783 0.8994

Table 2

Table 2. Remobilization efficiency (%) within the wood produced the first two years after planting in 4-year-old trees. Different letters in the same row indicate significant differences between treatments (P < 0.05). Treatment C +K +Na Nutrient K Ring 1 80.7 10.3 92.5 3.8 78.8 4.2 Ring 2 80.6 7.1 87.3 3.2 76.2 21.8 Na Ring 1 70.2 8.1 66.1 22.2 71.0 5.3 Ring 2 78.2 5.9 70.1 3.5 73.8 12.9 P Ring 1 76.5 13.5 a 94.2 1.4 b 92.8 1.3 b Ring 2 91.0 3.0 91.5 2.3 75.0 19.3 Ca Ring 1 -78.8 53.5 -18.4 28.2 13.2 10.6 30.8 16.1 Ring 2 33.0 12.2 43.3 16.1 Mg Ring 1 30.6 6.1 42.6 28.6 49.3 15.9 52.2 10.4 Ring 2 58.2 10.7 72.2 8.4 -1 C: no K and Na addition; +K: application of 3.0 kmol K ha ; +Na: application of 3.0 kmol Na ha-1.

Table 3

Table 3. Net remobilizations (expressed in mol ha-1) of K, Na, P, Ca and Mg in annual rings of Eucalyptus grandis trees the first 4 years after planting.
Treatment Stand age (yrs) K Ring 1 Ring 2 Ring 3 Total K remobilized Na Ring 1 Ring 2 Ring 3 Total Na remobilized P Ring 1 Ring 2 Ring 3 Total P remobilized Ca Ring 1 Ring 2 Ring 3 Total Ca remobilized Mg Ring 1 Ring 2 Ring 3 Total Mg remobilized 15 5 28 33 9 54 62 1 17 18 6 -2 4 0 15 15 8 183 203 394 4 69 66 140 0 16 35 51 -7 35 19 47 2 38 61 101 28 211 203 68 54 457 510 5 -15 -10 4 46 49 24 30 54 14 121 135 9 322 358 689 11 131 129 271 0 25 39 64 -31 58 43 70 -7 74 51 118
-1

C 1-2 2-3 3-4 1-4 1-2 2-3

+K 3-4 1-4 131 778 358 1-2 22

+Na 2-3 3-4 9 68 77 13 191 205 1 27 29 13 6 19 2 34 36 5 179 296 480 2 109 201 312 0 6 31 37 -4 24 62 82 0 15 97 112

1-4 36 248 296

15 -2

68 11 123 66 1

22 18 115 129 11

26 301 201

-2 2

1 3 33 35 10

11 13 71 39 4

5 33 31

2 -9

10 -10 33 19 -1

4 -8 88 43 -6

3 30 62

-9 1

-1 3 53 61 17

-6 24 195 51 6

7 49 97

17

C: no K and Na addition; +K: application of 3.0 kmol K ha ; +Na: application of 3.0 kmol Na ha-1.